Evidence for socially influenced and potentially actively coordinated cooperation by bumblebees.

Cooperation is common in animals, yet the specific mechanisms driving collaborative behaviour in different species remain unclear. We investigated the proximate mechanisms underlying the cooperative behaviour of bumblebees in two different tasks, where bees had to simultaneously push a block in an arena or a door at the end of a tunnel for access to reward. In both tasks, when their partner's entry into the arena/tunnel was delayed, bees took longer to first push the block/door compared with control bees that learned to push alone. In the tunnel task, just before gaining access to reward, bees were more likely to face towards their partner than expected by chance or compared with controls. These results show that bumblebees' cooperative behaviour is not simply a by-product of individual efforts but is socially influenced. We discuss how bees' turning behaviours, e.g. turning around before first reaching the door when their partner was delayed and turning back towards the door in response to seeing their partner heading towards the door, suggest the potential for active coordination. However, because these behaviours could also be interpreted as combined responses to social and secondary reinforcement cues, future studies are needed to help clarify whether bumblebees truly use active coordination.

The role of cognition in nesting.

For many animals, nests are essential for reproductive success. Nesting individuals need to carry out a range of potentially challenging tasks, from selecting an appropriate site and choosing suitable materials to constructing the nest and defending it against competitors, parasites and predators. Given the high fitness stakes involved, and the diverse impacts both the abiotic and social environment can have on nesting success, we might expect cognition to facilitate nesting efforts. This should be especially true under variable environmental conditions, including those changing due to anthropogenic impacts. Here, we review, across a wide range of taxa, evidence linking cognition to nesting behaviours, including selection of nesting sites and materials, nest construction, and nest defence. We also discuss how different cognitive abilities may increase an individual's nesting success. Finally, we highlight how combining experimental and comparative research can uncover the links between cognitive abilities, nesting behaviours and the evolutionary pathways that may have led to the associations between them. In so doing, the review highlights current knowledge gaps and provides suggestions for future research. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Glyphosate and a glyphosate-based herbicide affect bumblebee gut microbiota.

Pollinator decline is one of the gravest challenges facing the world today, and the overuse of pesticides may be among its causes. Here, we studied whether glyphosate, the world's most widely used pesticide, affects the bumblebee gut microbiota. We exposed the bumblebee diet to glyphosate and a glyphosate-based herbicide and quantified the microbiota community shifts using 16S rRNA gene sequencing. Furthermore, we estimated the potential sensitivity of bee gut microbes to glyphosate based on previously reported presence of target enzyme. Glyphosate increased, whereas the glyphosate-based herbicide decreased gut microbiota diversity, indicating that negative effects are attributable to co-formulants. Both glyphosate and the glyphosate-based herbicide treatments significantly decreased the relative abundance of potentially glyphosate-sensitive bacterial species Snodgrasella alvi. However, the relative abundance of potentially glyphosate-sensitive Candidatus Schmidhempelia genera increased in bumblebees treated with glyphosate. Overall, 50% of the bacterial genera detected in the bee gut microbiota were classified as potentially resistant to glyphosate, while 36% were classified as sensitive. Healthy core microbiota have been shown to protect bees from parasite infections, change metabolism, and decrease mortality. Thus, the heavy use of glyphosate-based herbicides may have implications on bees and ecosystems.

Oral exposure to thiacloprid-based pesticide (Calypso SC480) causes physical poisoning symptoms and impairs the cognitive abilities of bumble bees.

BACKGROUND: Pesticides are identified as one of the major reasons for the global pollinator decline. However, the sublethal effects of pesticide residue levels found in pollen and nectar on pollinators have been studied little. The aim of our research was to study whether oral exposure to the thiacloprid levels found in pollen and nectar affect the learning and long-term memory of bumble bees. We tested the effects of two exposure levels of thiacloprid-based pesticide (Calypso SC480) on buff-tailed bumble bee (Bombus terrestris) in laboratory utilizing a learning performance and memory tasks designed to be difficult enough to reveal large variations across the individuals. RESULTS: The lower exposure level of the thiacloprid-based pesticide impaired the bees' learning performance but not long-term memory compared to the untreated controls. The higher exposure level caused severe acute symptoms, due to which we were not able to test the learning and memory. CONCLUSIONS: Our results show that oral exposure to a thiacloprid-based pesticide, calculated based on residue levels found in pollen and nectar, not only causes sublethal effects but also acute lethal effects on bumble bees. Our study underlines an urgent demand for better understanding of pesticide residues in the environment, and of the effects of those residue levels on pollinators. These findings fill the gap in the existing knowledge and help the scientific community and policymakers to enhance the sustainable use of pesticides.

Ecological and evolutionary consequences of selective interspecific information use.

Recent work has shown that animals frequently use social information from individuals of their own species as well as from other species; however, the ecological and evolutionary consequences of this social information use remain poorly understood. Additionally, information users may be selective in their social information use, deciding from whom and how to use information, but this has been overlooked in an interspecific context. In particular, the intentional decision to reject a behaviour observed via social information has received less attention, although recent work has indicated its presence in various taxa. Based on existing literature, we explore in which circumstances selective interspecific information use may lead to different ecological and coevolutionary outcomes between two species, such as explaining observed co-occurrences of putative competitors. The initial ecological differences and the balance between the costs of competition and the benefits of social information use potentially determine whether selection may lead to trait divergence, convergence or coevolutionary arms race between two species. We propose that selective social information use, including adoption and rejection of behaviours, may have far-reaching fitness consequences, potentially leading to community-level eco-evolutionary outcomes. We argue that these consequences of selective interspecific information use may be much more widespread than has thus far been considered.

Field-realistic acute exposure to glyphosate-based herbicide impairs fine-color discrimination in bumblebees.

Pollinator decline is a grave challenge worldwide. One of the main culprits for this decline is the widespread use of, and pollinators' chronic exposure to, agrochemicals. Here, we examined the effect of a field-realistic dose of the world's most commonly used pesticide, glyphosate-based herbicide (GBH), on bumblebee cognition. We experimentally tested bumblebee (Bombus terrestris) color and scent discrimination using acute GBH exposure, approximating a field-realistic dose from a day's foraging in a patch recently sprayed with GBH. In a 10-color discrimination experiment with five learning bouts, GBH treated bumblebees' learning rate fell to zero by third learning bout, whereas the control bees increased their performance in the last two bouts. In the memory test, the GBH treated bumblebees performed to near chance level, indicating that they had lost everything they had learned during the learning bouts, while the control bees were performing close to the level in their last learning bout. However, GBH did not affect bees' learning in a 2-color or 10-odor discrimination experiment, which suggests that the impact is limited to fine color learning and does not necessarily generalize to less specific tasks or other modalities. These results indicate that the widely used pesticide damages bumblebees' fine-color discrimination, which is essential to the pollinator's individual success and to colony fitness in complex foraging environments. Hence, our study suggests that acute sublethal exposure to GBH poses a greater threat to pollination-based ecosystem services than previously thought, and that tests for learning and memory should be integrated into pesticide risk assessment.

Prior associations affect bumblebees' generalization performance in a tool-selection task.

A small brain and short life allegedly limit cognitive abilities. Our view of invertebrate cognition may also be biased by the choice of experimental stimuli. Here, the stimuli (color) pairs used in the match-to-sample tasks affected the performance of buff-tailed bumblebees (Bombus terrestris). We trained the bees to roll a tool, a ball, to a goal that matched its color. Bees trained with a yellow-and-orange/red stimuli pair took more training bouts to reach our color-matching criterion than those trained with a blue-and-yellow stimuli pair. When assessing the bees' concept learning ability in a transfer test with a novel color, the bees trained with blue and yellow (novel color: orange/red) were highly successful, the bees trained with blue and orange/red (novel color: yellow) did not differ from random, and those trained with yellow and orange/red (novel color: blue) failed the test. These results highlight that stimulus salience can affect our conclusions on test subjects' cognitive ability. Therefore, we encourage paying attention to stimulus salience (among other factors) when assessing the cognition of invertebrates.

Conceptual preferences can be transmitted via selective social information use between competing wild bird species.

Concept learning is considered a high-level adaptive ability. Thus far, it has been studied in laboratory via asocial trial and error learning. Yet, social information use is common among animals but it remains unknown whether concept learning by observing others occurs. We tested whether pied flycatchers (Ficedula hypoleuca) form conceptual relationships from the apparent choices of nest-site characteristics (geometric symbol attached to the nest-box) of great tits (Parus major). Each wild flycatcher female (n = 124) observed one tit pair that exhibited an apparent preference for either a large or a small symbol and was then allowed to choose between two nest-boxes with a large and a small symbol, but the symbol shape was different to that on the tit nest. Older flycatcher females were more likely to copy the symbol size preference of tits than yearling flycatcher females when there was a high number of visible eggs or a few partially visible eggs in the tit nest. However, this depended on the phenotype, copying switched to rejection as a function of increasing body size. Possibly the quality of and overlap in resource use with the tits affected flycatchers' decisions. Hence, our results suggest that conceptual preferences can be horizontally transmitted across coexisting animals, which may increase the performance of individuals that use concept learning abilities in their decision-making.

Illusional Perspective across Humans and Bees.

For two centuries, visual illusions have attracted the attention of neurobiologists and comparative psychologists, given the possibility of investigating the complexity of perceptual mechanisms by using relatively simple patterns. Animal models, such as primates, birds, and fish, have played a crucial role in understanding the physiological circuits involved in the susceptibility of visual illusions. However, the comprehension of such mechanisms is still a matter of debate. Despite their different neural architectures, recent studies have shown that some arthropods, primarily Hymenoptera and Diptera, experience illusions similar to those humans do, suggesting that perceptual mechanisms are evolutionarily conserved among species. Here, we review the current state of illusory perception in bees. First, we introduce bees' visual system and speculate which areas might make them susceptible to illusory scenes. Second, we review the current state of knowledge on misperception in bees (Apidae), focusing on the visual stimuli used in the literature. Finally, we discuss important aspects to be considered before claiming that a species shows higher cognitive ability while equally supporting alternative hypotheses. This growing evidence provides insights into the evolutionary origin of visual mechanisms across species.

Quantitative abilities of invertebrates: a methodological review.

Quantitative abilities are widely recognized to play important roles in several ecological contexts, such as foraging, mate choice, and social interaction. Indeed, such abilities are widespread among vertebrates, in particular mammals, birds, and fish. Recently, there has been an increasing number of studies on the quantitative abilities of invertebrates. In this review, we present the current knowledge in this field, especially focusing on the ecological relevance of the capacity to process quantitative information, the similarities with vertebrates, and the different methods adopted to investigate this cognitive skill. The literature argues, beyond methodological differences, a substantial similarity between the quantitative abilities of invertebrates and those of vertebrates, supporting the idea that similar ecological pressures may determine the emergence of similar cognitive systems even in distantly related species.

Non-numerical strategies used by bees to solve numerical cognition tasks.

We examined how bees solve a visual discrimination task with stimuli commonly used in numerical cognition studies. Bees performed well on the task, but additional tests showed that they had learned continuous (non-numerical) cues. A network model using biologically plausible visual feature filtering and a simple associative rule was capable of learning the task using only continuous cues inherent in the training stimuli, with no numerical processing. This model was also able to reproduce behaviours that have been considered in other studies indicative of numerical cognition. Our results support the idea that a sense of magnitude may be more primitive and basic than a sense of number. Our findings highlight how problematic inadvertent continuous cues can be for studies of numerical cognition. This remains a deep issue within the field that requires increased vigilance and cleverness from the experimenter. We suggest ways of better assessing numerical cognition in non-speaking animals, including assessing the use of all alternative cues in one test, using cross-modal cues, analysing behavioural responses to detect underlying strategies, and finding the neural substrate.

Foraging Bumblebees Selectively Attend to Other Types of Bees Based on Their Reward-Predictive Value.

Using social information can be an efficient strategy for learning in a new environment while reducing the risks associated with trial-and-error learning. Whereas social information from conspecifics has long been assumed to be preferentially attended by animals, heterospecifics can also provide relevant information. Because different species may vary in their informative value, using heterospecific social information indiscriminately can be ineffective and even detrimental. Here, we evaluated how selective use of social information might arise at a proximate level in bumblebees (Bombus terrestris) as a result of experience with demonstrators differing in their visual appearance and in their informative value as reward predictors. Bumblebees were first trained to discriminate rewarding from unrewarding flowers based on which type of "heterospecific" (one of two differently painted model bees) was next to each flower. Subsequently, these bumblebees were exposed to a novel foraging context with two live painted bees. In this novel context, observer bumblebees showed significantly more social information-seeking behavior towards the type of bees that had predicted reward during training. Bumblebees were not attracted by paint-marked small wooden balls (moved via magnets) or paint-marked non-pollinating heterospecifics (woodlice; Porcellio laevis) in the novel context, indicating that bees did not simply respond to conditioned color cues nor to irrelevant social cues, but rather had a "search image" of what previously constituted a valuable, versus invaluable, information provider. The behavior of our bumblebees suggests that their use of social information is governed by learning, is selective, and extends beyond conspecifics.

Bumblebees Use Sequential Scanning of Countable Items in Visual Patterns to Solve Numerosity Tasks.

Most research in comparative cognition focuses on measuring if animals manage certain tasks; fewer studies explore how animals might solve them. We investigated bumblebees' scanning strategies in a numerosity task, distinguishing patterns with two items from four and one from three, and subsequently transferring numerical information to novel numbers, shapes, and colors. Video analyses of flight paths indicate that bees do not determine the number of items by using a rapid assessment of number (as mammals do in "subitizing"); instead, they rely on sequential enumeration even when items are presented simultaneously and in small quantities. This process, equivalent to the motor tagging ("pointing") found for large number tasks in some primates, results in longer scanning times for patterns containing larger numbers of items. Bees used a highly accurate working memory, remembering which items have already been scanned, resulting in fewer than 1% of re-inspections of items before making a decision. Our results indicate that the small brain of bees, with less parallel processing capacity than mammals, might constrain them to use sequential pattern evaluation even for low quantities.

Bumblebees show cognitive flexibility by improving on an observed complex behavior.

We explored bees' behavioral flexibility in a task that required transporting a small ball to a defined location to gain a reward. Bees were pretrained to know the correct location of the ball. Subsequently, to obtain a reward, bees had to move a displaced ball to the defined location. Bees that observed demonstration of the technique from a live or model demonstrator learned the task more efficiently than did bees observing a "ghost" demonstration (ball moved via magnet) or without demonstration. Instead of copying demonstrators moving balls over long distances, observers solved the task more efficiently, using the ball positioned closest to the target, even if it was of a different color than the one previously observed. Such unprecedented cognitive flexibility hints that entirely novel behaviors could emerge relatively swiftly in species whose lifestyle demands advanced learning abilities, should relevant ecological pressures arise.

Correction: Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect.

[This corrects the article DOI: 10.1371/journal.pbio.1002564.].

Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect.

Social insects make elaborate use of simple mechanisms to achieve seemingly complex behavior and may thus provide a unique resource to discover the basic cognitive elements required for culture, i.e., group-specific behaviors that spread from "innovators" to others in the group via social learning. We first explored whether bumblebees can learn a nonnatural object manipulation task by using string pulling to access a reward that was presented out of reach. Only a small minority "innovated" and solved the task spontaneously, but most bees were able to learn to pull a string when trained in a stepwise manner. In addition, naïve bees learnt the task by observing a trained demonstrator from a distance. Learning the behavior relied on a combination of simple associative mechanisms and trial-and-error learning and did not require "insight": naïve bees failed a "coiled-string experiment," in which they did not receive instant visual feedback of the target moving closer when tugging on the string. In cultural diffusion experiments, the skill spread rapidly from a single knowledgeable individual to the majority of a colony's foragers. We observed that there were several sequential sets ("generations") of learners, so that previously naïve observers could first acquire the technique by interacting with skilled individuals and, subsequently, themselves become demonstrators for the next "generation" of learners, so that the longevity of the skill in the population could outlast the lives of informed foragers. This suggests that, so long as animals have a basic toolkit of associative and motor learning processes, the key ingredients for the cultural spread of unusual skills are already in place and do not require sophisticated cognition.

Active hiding of social information from information-parasites.

BACKGROUND: Coevolution between pairs of different kind of entities, such as providers and users of information, involves reciprocal selection pressures between them as a consequence of their ecological interaction. Pied flycatchers (Ficedula hypoleuca) have been shown to derive fitness benefits (larger clutches) when nesting in proximity to great tits (Parus major), presumably because they this way discover and obtain information about nesting sites. Tits suffer from the resulting association (smaller clutches). An arms race between the tits (information host) and the flycatchers (information parasite) could thus result. Great tits often cover eggs with nesting material before, but not during incubation. We hypothesized that one function of egg-covering could be a counter-adaptation to reduce information parasitism by pied flycatchers. We predicted that tits should bring more new hair to cover their exposed eggs when a pied flycatcher is present near to tit nest than when a neutral (non-competing) species is present. We conducted decoy and playback experiment in Oulu and Turku, Finland. First, we removed and collected all the hair covering the tit eggs. Then, we measured how the perceived presence of flycatcher or waxwing (Bombycilla garrulus) affects tits' egg-covering by collecting and weighing the hair brought on the eggs and photographing the nest 24 h after the playback. RESULTS: Tits brought more hair into the nest and covered the eggs more carefully after flycatcher treatment, compared to waxwing treatment. We also found that the tits in Oulu (over 600 km to north from Turku) had more hair on the top of their eggs in general. CONCLUSIONS: Together, these results suggest that the counter-adaptation function of egg-covering against information parasites may be an extension of original function to protect eggs from low temperatures.

Observed fitness may affect niche overlap in competing species via selective social information use.

Social information transmission is important because it enables horizontal spread of behaviors, not only between conspecifics but also between individuals of different species. Because interspecific social information use is expected to take place among species with similar resource needs, it may have major consequences for the emergence of local adaptations, resource sharing, and community organization. Social information use is expected to be selective, but the conditions promoting it in an interspecific context are not well known. Here, we experimentally test whether pied flycatchers (Ficedula hypoleuca) use the clutch size of great tits (Parus major) in determining the quality of the observed individual and use it as a basis of decision making. We show that pied flycatchers copied or rejected a novel nest site feature preference of great tits experimentally manipulated to exhibit high or low fitness (clutch size), respectively. Our results demonstrate that the social transmission of behaviors across species can be highly selective in response to observed fitness, plausibly making the phenomenon adaptive. In contrast with the current theory of species coexistence, overlap between realized niches of species could dynamically increase or decrease depending on the observed success of surrounding individuals.

How does variation in the environment and individual cognition explain the existence of consistent behavioral differences?

According to recent studies on animal personalities, the level of behavioral plasticity, which can be viewed as the slope of the behavioral reaction norm, varies among individuals, populations, and species. Still, it is conceptually unclear how the interaction between environmental variation and variation in animal cognition affect the evolution of behavioral plasticity and expression of animal personalities. Here, we (1) use literature to review how environmental variation and individual variation in cognition explain population and individual level expression of behavioral plasticity and (2) draw together empirically yet nontested, conceptual framework to clarify how these factors affect the evolution and expression of individually consistent behavior in nature. The framework is based on simple principles: first, information acquisition requires cognition that is inherently costly to build and maintain. Second, individual differences in animal cognition affect the differences in behavioral flexibility, i.e. the variance around the mean of the behavioral reaction norm, which defines plasticity. Third, along the lines of the evolution of cognition, we predict that environments with moderate variation favor behavioral flexibility. This occurs since in those environments costs of cognition are covered by being able to recognize and use information effectively. Similarly, nonflexible, stereotypic behaviors may be favored in environments that are either invariable or highly variable, since in those environments cognition does not give any benefits to cover the costs or cognition is not able to keep up with environmental change, respectively. If behavioral plasticity develops in response to increasing environmental variability, plasticity should dominate in environments that are moderately variable, and expression of animal personalities and behavioral syndromes may differ between environments. We give suggestions how to test our hypothesis and propose improvements to current behavioral testing protocols in the field of animal personality.